Risk of Colloidal and Pseudo-colloidal Transport of Actinides in Nitrate Contaminated Groundwater nearby radioactive waste repository after bioremediation

doi:10.21203/rs.3.rs-348977/v1

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Risk of Colloidal and Pseudo-colloidal Transport of Actinides in Nitrate Contaminated Groundwater nearby radioactive waste repository after bioremediation

https://doi.org/10.21203/rs.3.rs-348977/v1

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The possible role of biogeochemical processes in colloidal and pseudo-colloidal U, Np and Pu transport during bioremediation of radionuclide- and nitrate contaminated groundwater was investigated. In two series of laboratory experiments with water samples taken from contaminated aquifer before and past bioremediation we found that microbial processes were able to cause coagulation of clayed, ferruginous and actinide colloids. The main mechanisms are: biogenic insoluble ferrous iron species formation (goethite, pyrrhotite, siderite, troilite, and ferrihydrite sediments), clay particles aggregation by biopolymers, and actinides immobilization in the cells, large biopolimers and iron and clayed sediments. This process results in a decreasing risk of colloidal and pseudo-colloidal transport of actinides.

Physical Chemistry

Electrochemistry

Analytical Chemistry

Actinides

in situ bioremediation

nitrates

colloidal transport

iron and clay particles

filtration

aggregation and coagulation PHREEQC

speciation modeling

Microbial stimulation causes formation of new mineral phases and U precipitation
Microbial processes may cause aggregation and coagulation of suspended particles
Clayed and ferruginous particles agrégation caused by biopolymers and cells
in situ bioremediation should prevent risk of actinide colloid transport

Improper operations of surface waste storages of radiochemical production plants and ore processing sites, subsurface uranium leaching, radiation accidents, and underground nuclear explosions may all cause the ingress of actinides into groundwater. In Russia, at a number of radiochemical plants, including the Siberian Chemical Combine (SCC) and Mining Chemical Combine, liquid radioactive waste (LRW) is disposed both in deep (250–350 m) collectors [1] and upper open repositories for solid sludges and tales [2, 3, 4]. Since nitrates of alkaline and alkaline-earth elements are the main components of radioactive wastes both in surface depositories and in deep collector layers, radionuclide migration occurs at elevated salt concentrations. The presence of nitrate ions and sulfate ions promotes the oxidative environment in aquifers and a consequent migration of actinides in a dissolved oxidized form [5]. Carbonates contained in the waste create the risks of migration of complex carbonate forms of actinides [6].

The mechanisms of colloidal and pseudo-colloidal transport of actinides under diverse geochemical conditions are of special interest [7, 8]. A number of studies indicate that colloidal transport may play a key role in uranium and plutonium migration both as true colloidal particles and as components of complex particles in ferruginous, clay, or organic complexes [9, 10, 11, 12, 13].

Penetration of nitrates and other components into the surface and submerged water-bearing aquifers may enhance the microbial processes [14, 15]. At some plants, the microbial community was stimulated with organic substrates in order to immobilize uranium and other radionuclides, and to remove nitrates [16; 17; 18]. Multiple studies on bioremediation of uranium-containing waters describe the “biogenic uraninite” form of uranium IV, commonly as a poorly soluble X-ray amorphous phase. [19, 20]. The formation of several biogenic phosphate phases is also noted [21]. However, no data on similar forms of plutonium and neptunium could be found. The role of biogeochemical processes in colloidal and pseudo-colloidal actinide transport remains insufficiently studied. Biogenic processes stimulated, e.g., by nitrate reduction, may result in stabilization of pseudo-colloidal actinide particles due to production of exopolysaccharide metabolites [22, 23] or biogenic nano colloidal uraninite [24]. The formation of biogenic ferruginous particles [25] may result in the occurrence of new actinide-transporting colloidal phases.

An aquifer nearby the mothballed SCC RW repository which is taken into consideration in the present study was polluted with nitrates and actinides. During 2014–2015, bioremediation of named aquifer was conducted. Bioremediation involved a single stimulation of microbial community with a mixture of acetate and whey. This led to a significant decrease in the redox potential of the system, and to a temporary decrease in nitrate ions concentration to values below the maximum allowable concentrations in in-place conditions [26]. Decreased uranium content was observed in samples taken after the bioremediation, however, precise assessment of uranium forms was impossible. Such results have shown promising perspectives of developing a biogeochemical barrier for radionuclides under conditions of the aquifer in consideration, given continuous stimulation of microbial community and formation of areas with reducing conditions so that elements are immobilized in poorly soluble form. Actinides migration in groundwater after bioremediation requires the development of the multifactor and multi-parametric models, which shall take the consequences of its mineral forms, oxidation states, and species in water, including colloid and pseudocolloides forms. The goal of the present work was to assess the role of metabolic products in water samples taken from aquifer where in-situ bioremediation was conducted previously. The role of named products is to be assessed in experiments that model the bioremediation process under conditions of stability of colloidal and pseudo-colloidal ferruginous and clayey phases containing plutonium, neptunium, and uranium.

Two water samples were taken from an aquifer located nearby the suspended surface RAW repository (Siberia, Russia) by means of observation wells (12m depth) after pumping one and a half well volumes. Sample 1 was taken from the area three years after the bioremediation process was conducted. Sample 2 was obtained in the same well before bioremediation. The values of pH, Eh, and salinity were determined at the time of sampling. Table 1 lists the parameters of the samples collected from upper aquifers (10–20 m).

Table 1

Parameters of the groundwater samples, mg/l
Well	1	2
pH	7,0	6.58
Eh	70	65
Oxidizability, mg O₂/L	0.86	13.10
Salinity	1970.0	3952.0
Fe(total)	1,3	0.25
Na⁺	257.0	604.0
K⁺	9.8	3.09
Ca²⁺	109.2	316.60
Mg²⁺	72,5	63.20
NH₄⁺	7.64	< 0,05
NO₃⁻	970.0	2517.0
SO₄²⁻	25,1	172.40
Cl⁻	5.37	4.52
HCO₃⁻	372.2	231.0
NO₂⁻	5.2	< 0.2
α- activity, Bq/L	0.55	12.59
β- activity, Bq/L	8.2	28.7

Molecular hydrogen was used as an electron donor in the first stage of research. After preliminary degassing, hydrogen was introduced into the vials instead of the gas phase. Carbonate ions in the formation fluid served as electron acceptors and as a source of carbon.

At the second stage of laboratory modeling, organic compounds were used as electron donors (1 g/L of sodium acetate and 1 g/l of glucose). Actinides (²³³U, ²³⁷Np, and ²³⁹Pu) were used in the concentrations of 10^− 8 M/l. Argon was used as the gas phase in the headspace. A low-mineral solution was used to model the water. Composition of named solution was as follows, mg/L: NaHCO₃ − 25.2; MgSO₄*7H₂O − 36.6; CaCl₂*6H₂O − 233.8; and MgCO₃ − 3.2. Sample from well 2 was used as the source of natural water (all model water samples were supplemented with 0.5 mL of natural water as a bacterial microcosm source). Some samples of model water were supplemented with bentonite clay (100 mg/L, 10th Khutor deposit, Khakassia) [27] and 10 mg/L FeCl₃. The composition of bentonite clay included 67% of montmorillonite, 6% kaolinite, and 3% illite. The complete list of solutions used in experiments and their designations is as following:

Model water (МW)
Model water + organic supplement (МWО)
Model water + clay (МWСl)
Model water + clay + organic supplement (МWСlО)
Model water + FeCl₃ (МWI)
Model water + FeCl₃ + organic supplement (МWIO)
Natural water (well 2) (NW)
Natural water (well 2) + organic supplement (NOW)

Analytical techniques. Concentrations of ²³³U and ²³⁹Pu were determined by alpha-spectrometry, ²³⁷Np concentration was determined by the luminescent method [28].

Carbohydrate determination was carried out by the phenol–sulfuric acid method according to Dubois [29]. Optical density was measured at 480 nm.

Cell numbers were determined by light microscopy (×1000).

Eh and pH were determined with an Anion ion meter using the relevant electrodes (Econix Expert).

Organic matter in the liquid was measured using an Elementar Vario EL III elemental analyzer.

The size of the cells, colloidal particles, and zeta potential were determined by the dynamic light scattering method using Photocor Compact-Z particle size and zeta potential analyzer. This method is based on measuring the temporal fluctuations in the scattered light intensity. Light scattering intensity was determined by Zetasizer Nano ZS, Malvern Panalytical.

Organic matter in the liquid was measured using an Elementar Vario EL III elemental analyzer. The size of colloidal particles in the model experiments was determined by step-by-step filtration with syringe-mounted Vladipor filters (2.4, 1.2, 0.8, 0.4, 0.22, 0.1, and 0.05 µm –in diameter).

The speciation of actinides in water samples was assessed by thermodynamic modeling in the PhreeqC 2.1software with llnl.dat thermodynamic database [30]. The saturation indices (SI) were determined as follows: SI = logIAP - logK_s, where IAP is a product of activities of the relevant ions and K_s is the equilibrium constant. At SI > 0 formation of the studied phase is predicted. The calculated content of each actinide element per sample was 500 µg.

The microbiological parameters of the collected samples (the number and taxonomic characteristics of microbial communities) were presented in previous articles [26, 31]. The presence of the following bacteria in aquifer samples was revealed: aerobic organotrophic, anaerobic fermenting, iron-reducing, and denitrifying bacteria of the phyla Proteobacteria (genera Acidovorax, Simplicispira, Thermomonas, Thiobacillus, Pseudomonas, Brevundimonas, and uncultured Oxalobacteraceae), Firmicutes (genera Bacillus and Paenibacillus), and Actinobacteria (Candidatus Planktophila, Gaiella).

1. Formation of Associative Colloids in water samples, stimulated by H₂

Analysis of total organic content in the groundwater samples before laboratory microbial activation showed its low concentration. For the sample taken from the aquifer area where microbial activation was conducted 3 years prior to the research, concentration did not exceed 15 mg/l. Respective concentration amounted to 5–7 mg/l in samples collected from an area which was not subject to microbial activation previously. Filtration studies (step-by-step filtration, Fig. 1) revealed that more than 50% of organic matter in the sample 1 was represented by suspended particles over 1200 nm in size. These were bacterial cells and other large particles (organic clay and ferrous particles, fulvic and humate acids, etc.).

An organic carbon content of 100 and 200 mg/L was observed in 1 and 2 samples respectively after microbial activation by molecular hydrogen. After day 14 of incubation of the sample 1, microbial processes resulted in decreased content of large organic particles (100–2400 nm) and increased content of the particles below 100 nm in size, which correspond to biogenic and associative colloids. The increase was the sharpest among the fraction of particles smaller than 10 nm (biogenic poly- and oligomers).

The amount of the particles 100–50 and 450–220 nm in size in sample 2 increased after microbial activation; these size ranges correspond to true biocolloidal particles. The contribution of large organic particles (associative colloids and cells) decreased significantly. In this sample, the share colloidal particles (100–50 nm) also increased, while the share of 220–100-nm particles decreased significantly, probably due to their consumption or aggregation into larger fractions. The shares of all large fractions decreased as well. Changes in the intensity of light scattering provided the most relevant information (Table 2).

Table 2

Intensity of light scattering (kHz) by particles of different fractions before and after day 14 of ongoing microbial process in the stratal water
Particle fraction size, nm	1 before	1 after	2 before	2 after
< 2400	28	300	39	100
2400 − 1200	30	47	42	143
1200 − 450	30	50	49	209
450 − 220	48	45	34	187
220 − 100	21	40	33	174
100 − 50	19	20	12	141
> 10	0,5	1,2	0,3	4

In sample 1, 450–220 nm particles (which probably represent clayey aggregates or ferruginous colloidal particles) accounted for the highest intensity. After microbial treatment, the share of other particles increased, and the largest particles (probably cells or agglomerated clayey particles) contributed to light scattering the most. The DLS data on the filtrate from the sample 2 indicates that the particles 1200 − 450 nm in size (likely clayey and iron-clayey aggregates) possibly dominated prior to microbial activation, meanwhile, afterward, intensity of light scattering by colloidal particles of all sizes increased; the 1200–450-nm particles remained predominant and comprised a significant share of medium-sized microbial cells.

2. Modelling of microbial process in the model and real samples with actinides

An increase in the size of particles containing organic matter could be explained by the occurrence of bacterial cells and biogenic particles like and clusters of macromolecules, e.g. proteins, exopolysaccharides, and by physicochemical processes, e.g. adhesion of organic matter to clay and ferruginous particles that cause enlargement and sedimentation of the particles. The second stage of the experiment was conducted in order to examine the mechanisms of the named process more thoroughly.

An increase in the concentration of the biomass, with peak values on day 15 and day 20 for model water and natural water respectively, was observed in samples with additions of organic matter (O) (Table 3).

Table 3

A) Polysaccharide concentrations (mg/L) in the model solutions during incubation. B) biomass (g/l) in the model solutions during incubation, Cell/mL.
Sample	Incubation time, days
	0		5		10		15		20			30
	A	B	A	B	A	B	A	B		A	B	A	B
МWО	0,1	0	2	0,2	13	0,24	27	0,19		25	0,12	19	0,04
МWСlО	0,11	0	3	0,13	15	0,3	29	0,25		21	0,12	13	0,04
МWIO	0,1	0	3	0,15	17	0,25	33	0,22		29	0,15	16	0,07
NWO	0,13	0	5	0,14	18	0,3	34	0,21		28	0,17	22	0,09

The concentration of polysaccharides in named samples also increased alongside. No significant increase of cells and polysaccharides content was recorded in samples with no organic matter additions.

The average hydrodynamic radii of colloidal particles were obtained on days 3, 7, 14, 21, and 28 of the experiment (Table 4). In model water samples without added organic compounds, colloidal particles were not formed. However, by the end of the experiment particle formation was observed, probably due to the transformation of colloidal matter originating from the natural water aliquot.

Table 4

Hydrodynamic radii of colloidal particles during experiment, nm.
Sample	Incubation time, days
Sample	5	10	15	20	30
МW	-	-	-	-	20
МWО	90	120	70	40, 170	110
МWСl	130	80	90	100	160
МWСlО	130, 25	130	100	100	110
МWI	130	130	100	100	110
МWIO	100	150	160	90	-
NW	75	100	120	120	140
NWO	50	75	90	170	400

In the presence of glucose, the emergence of the colloidal phase and a gradual increase in particle size were observed since the third day of incubation. The average stable hydrodynamic radii of the particles amounted to ~ 100 nm. In the presence of clay, stable colloids with the average hydrodynamic radii of 80–90 nm were formed. Stimulation of microbial processes with glucose resulted in increased particle size and partial sedimentation.

The addition of iron to the model system resulted in the formation of the particles with hydrodynamic radii of ~ 100 nm; the stimulation of the biological processes resulted in increased particle size, the formation of new particles (by day 21), and complete particle sedimentation by day 28.

High diversity in particle size and its gradual, uniform increase were observed in samples without the addition of organic compounds. Under conditions of microbial processes, an increase in particle size was not uniform, and relatively large stable particles (395 nm) were observed at the end of the experiment.

An important parameter used to evaluate the stability of colloidal particles in the system is value of particles’ zeta potential. When no organic matter was added, charge of preliminarily filtered 100 − 50 nm particles equaled − 29, -26.2 mV in model water and − 16, -12 mV in natural water, which indicates low stability of such particles (see Table 1 Supplementary). A shift in charge of particles towards zero and positive values was observed when microbial processes were running, and this hints at stabilization of particles in the solution.

The diagrams of actinide distribution by size of colloidal particles in solutions of different nature depending on the incubation time are shown in Fig. 2.

In the model water Pu(IV) forms true colloidal associates (up to 50%) due to deep hydrolytic polymerization. Np(V) was also partially sorbed due to slight disproportionation (by 10%). U(VI) was a stable component of soluble carbonate complexes. In the model water, increased pH and decreased Eh result in the occurrence of 99% Pu, 30% Np, and 10% U within large colloidal particles. Ultrafiltration, however, is not suitable for the assessment of the possible actinide reduction and biosorption contribution to the process of colloid formation.

The microbiota and clay promote stabilization of plutonium and uranium, but not neptunium, in large colloidal particles. The addition of iron had no effect on actinide colloid formation, although iron caused a significant increase in neptunium colloid formation in the presence of the microbiota.

Thus, microbial processes may result in the coagulation of natural colloids due to the development of a weak negative surface charge. The addition of bivalent cations (e.g., Сa²⁺, Mg²⁺) during bioremediation should potentiate this process and may become an efficient mechanism for decreasing the risk of active migration of radionuclide-associated particles.

After termination of the biogenic processes, the formation of large uranium-, plutonium-, and neptunium-containing particles associated with cells [32] and large biopolymers (protein-polysaccharide biofilms) [33, 34] polysaccharide-clay and polysaccharide-iron sediments was observed. This results in decreased migration activity of the actinides. Moreover, it is well known that the nucleation process of biogenic iron oxyhydroxides, leading to their mineralization, is closely related to the organic matter of exopolysaccharides of biofilms Microbial polymers can, through strong mineral binding (high f_eq), decrease the nucleation barriers for ferrihydrite and direct nucleation on the polymers [35]. The mineralization process in microbial exopolysaccharide sediments of iron and associated actinides can serve as a reliable anti-migration biogeochemical barrier, an important consequence of bioremediation.

3. Thermodynamical modeling of the Species of Radionuclide Occurrence in the Course of Biotransformation

The data on pH and Eh changes along the process of colloid formation and actinide incorporation into associative particles (and possibly into true colloidal particles as well) are listed in Table 2 (supplementary).

The most notable pH and Eh changes occurred in the presence of the microbiota, which was probably due to increasing in the number of bacteria. The pH increased moderately, while Eh values changed to negative, potentially creating the conditions for a shift of actinides’ oxidation states to lower ones. Since Ac(IV) is the most sorbed form of actinides, this may promote their association with colloidal materials of various nature [36].

Speciation of elements, including dissolved species and the phase saturation indices, was calculated for 500 µg/L U, Pu, and Np in the Sample NVO (natural sample 2) (Table 5). The species of actinides and iron after microbial processes were calculated with an account for the following parameter changes: pH increase by 1, Eh decrease by 100 mV, complete denitrification, and sulfate reduction.

Table 5

The major species of actinides and iron in the water from lower aquifer contaminated with radioactive nitrate waste, after microbial treatment
Sample 2, before
	U	Np	Pu	Fe
Dissolved species, M	U(OH)₄ 1.6×10^− 8 UO₂⁺ 1.07×10^− 10 UO₂(CO₃)₂⁻² 1.13×10^− 6 UO₂(CO₃)₃⁻⁴ 7.8×10^− 7 UO₂CO₃ 9.4×10^− 8 UO₂(OH)₂ 3.8×10^− 8 (UO₂)₂CO₃(OH)₃⁻ 1.4×10^− 8	Np(OH)₄ 1.9×10^− 6 Np(OH)₃⁺ 2.7×10^− 9 NpO₂⁺ 2.0×10^− 7 NpO₂CO₃⁻ 9.8×10^− 10 NpO₂OH 3.5×10^− 10	PuSO₄⁺ 2.09×10^− 7 Pu(SO₄)₂⁻ 4.2×10^− 8 PuOH^+ 2 8.1×10^− 9 Pu(OH)₄ 1.3×10^− 7	FeHCO₃⁺ 2.1×10^− 6 FeSO₄ 4.1×10^− 8 FeCO₃ 3.1×10^− 8 FeOH⁺ 1.5×10^− 9
Phase, SI	UO_2.25(beta) 1.39 UO_2.3333(beta) 2.36 Uraninite UO₂ 1.57	Np(OH)₄ 2.63 NpO₂ 11.48	Pu(OH)₄ 2.19 PuO₂ 10.48	Goethite 0.59 Hematite 2.11

	Sample 2, after
Dissolved species, M	Solution
	Fe	Np		U	Pu
	FeHCO₃⁺ 1.9×10^− 6 FeCO₃ 1.6×10^− 6 FeOH⁺ 3.6×10^− 8 Fe(OH)₃ 3.9×10^− 9 Fe(OH)₄⁻ 2.4×10^− 10	Np(OH)₄ 2.1×10^− 6 Np(CO₃)₅⁻⁶ 1.8×10^− 10 NpO₂⁺ 2.4×10^− 10 NpO₂CO₃⁻ 1.4×10^− 10		U(OH)₄ 3.0×10^− 8 UO₂(CO₃)₃⁻⁴ 2.0×10^− 6 UO₂(CO₃)₂⁻² 3.4×10^− 8	PuOH^+ 2 6.0×10^− 10 Pu(OH)₄ 2.1×10^− 6 Pu(OH)₃⁺ 2.2×10^− 10
	Phases
Phase, SI	Phase	SI	Np(OH)₄ 2.67			UO_2.25 1.14
	Calcite 1.66	Huntite 1.73	NpO₂ 11.53			UO_2.25(beta) 1.06
	Aragonite 1.52	Magnesite 0.58	Pu(OH)₄ 3.38			UO_2.3333(beta) 1.30
	Dolomite 3.97	Monohydrocalcite 0.86	PuO₂ 11.67			Uraninite 1.84

Due to thermodynamical modeling experiments after microbial processes, ferrous iron in hydroxide sulphide and carbonate forms were formed, and precipitation of goethite, pyrrhotite, siderite, troilite, and ferrihydrite mineral phases occurred [37, 38, 39, 40]. These new sorption phases could cause additional actinide removal from solutions [41, 42, 43, 44, 45].

Prior to microbial treatment, uranium was expected to be present as di- and tricarbonate complexes. Neptunium occurred as a neptunoyl ion or, as a relatively poorly soluble hydroxo complex. Plutonium was expected to occur as sulfate and as hydroxo complex. Microbial processes resulted in uranium remaining as a tricarbonate complex ore as a poorly soluble hydroxide. Plutonium and neptunium were present in all aquifers as oxyhydroxides, which can be attached to mineral surfaces and various hydroxyl phases [46, 47].

It is important to note that microbial processes resulted in the more extensive formation of poorly soluble phases like uraninite (UO₂, NpO₂, PuO₂). Microbial processes led to occurrence of ferrous iron carbonates and hydrocarbonates, and to the precipitation of goethite, pyrrhotite, siderite, troilite, and ferrihydrite mineral phases. These new sorption phases may result in additional actinide recovery from solutions.

Microbial processes were able to cause coagulation of environmental colloids due to the formation of a weakly negative surface charge. The addition of bivalent cations (e.g., Сa²⁺, Mg²⁺) during bioremediation should potentiate this process and may become an efficient mechanism for decreasing the risk of active migration of radionuclide-associated particles [48, 49].

After the termination of biogenic processes, large particles containing uranium, neptunium, and plutonium and associated with the cells and large biopolymers (protein-polysaccharide biofilms) were observed. The occurrence of such particles results in decreased migration activity of the metals. Aggregation of actinide complexes with organic and inorganic colloidal particles in the course of microbial activation results in increased particle size and may hinder their migration in the groundwater-bearing aquifers.

This work was supported by State Assignments. 0137-2019-0010 and АААА-А16-11611091001

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Compliance with Ethical Standards

This research does not contain any studies with human participants or animals performed by any of the authors.

Authors can confirm that all relevant data are included in the article and/or its supplementary information files

Author contributions

A. Safonov, Conceptualization, Investigation, Writing – original draft

E. Lavrinovich, Formal analysis, Investigation

A. Emel'yanov, Formal analysis, Investigation

K. Boldyrev, Formal analysis

V. Kuryakov, Investigation

N. Rodygina, Investigation

E. Zakharova, Conceptualization, Writing – original draft, Supervision

A. Novikov Conceptualization, Writing – original draft, Supervision

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Risk of Colloidal and Pseudo-colloidal Transport of Actinides in Nitrate Contaminated Groundwater nearby radioactive waste repository after bioremediation

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Introduction

Materials And Methods

Results And Discussion

2. Modelling of microbial process in the model and real samples with actinides

3. Thermodynamical modeling of the Species of Radionuclide Occurrence in the Course of Biotransformation

Conclusions

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